Metabolic and evolutionary patterns in the extremely acidophilic archaeon Ferroplasma acidiphilum YT

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Golyshina, Olga V ^a   Tran, Hai ^a   Reva, Oleg N ^b   Lemak, Sofia ^c   Yakunin, Alexander F ^c   Goesmann, Alexander ^d,k   Nechitaylo, Taras Y ^e   Lacono, Violetta ^f   Smedile, Francesco ^f   Slesarev, Alexei ^g   Rojo, David ^h   Barbas, Coral ^h   Ferrer, Manuel ⁱ   Yakimov, Michail M ^f,j   Golyshin, Peter N ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF TORONTO   (Canada)

^d BIELEFELD UNIVERSITY   (Germany)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^f CNR   (Italy)

^g Zylacta Corporation   (United States)

^h UNIVERSIDAD SAN PABLO CEU   (Spain)

ⁱ CSIC   (Spain)

^j IMMANUEL KANT BALTIC FEDERAL UNIVERSITY   (Russian Federation)

^k JUSTUS LIEBIG UNIVERSITY   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON; CARBON DIOXIDE;

ARCHAEAL GENOME; ARCHAEON; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; ENERGY METABOLISM; EVOLUTION; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETICS; GENOMICS; METABOLISM; MISMATCH REPAIR; MOLECULAR EVOLUTION; MUTATION; PROCEDURES;

AMINO ACIDS; ARCHAEA; BIOLOGICAL EVOLUTION; CARBON; CARBON DIOXIDE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; DNA MISMATCH REPAIR; ENERGY METABOLISM; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENOME, ARCHAEAL; GENOMICS; METABOLIC NETWORKS AND PATHWAYS; MUTATION; RECOMBINATION, GENETIC;

EID: 85020945306     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-03904-5     Document Type: Article

References (68)

1. Golyshina, O. V. et al. Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing,cell-walllacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 3, 997-1006 (2000).
2. Golyshina, O. V. & Timmis, K. N. Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments. Environ Microbiol 7, 1277-1288 (2005).
3. Golyshina, O. V. Environmental, biogeographic, and biochemical patterns of archaea of the family Ferroplasmaceae. Appl Environ Microbiol 77, 5071-5078 (2011).
4. Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 37-43 (2004).
5. Dopson, M., Baker-Austin, C., Hind, A., Bowman, J. P. & Bond, P. L. Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol 70, 2079-2088 (2004).
6. Banfield, J. F., Verberkmoes, N. C., Hettich, R. L. & Thelen, M. P. Proteogenomic approaches for the molecular characterization of natural microbial communities. OMICS 9, 301-333 (2005).
7. Golyshina, O. V., Golyshin, P. N., Timmis, K. N. & Ferrer, M. The 'pH optimum anomaly' of intracellular enzymes of Ferroplasma acidiphilum. Environ Microbiol 8, 416-425 (2006).
8. Ferrer, M., Golyshina, O. V., Beloqui, A., Golyshin, P. N. & Timmis, K. N. The cellular machinery of Ferroplasma acidiphilum is ironprotein-dominated. Nature 445, 91-94 (2007).
9. Ferrer, M. et al. A purple acidophilic di-ferric DNA ligase from Ferroplasma. Proc Natl Acad Sci USA 105, 8878-8883 (2008).
10. Allen, E. E. et al. Genome dynamics in a natural archaeal population. Proc Natl Acad Sci USA 104, 1883-1888 (2007).
11. Goris, J. et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57, 81-91 (2007).
12. Meier-Kolthoff, J. P., Auch, A. F., Klenk, H. P. & Goker, M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14, 60 (2013).
13. Bezuidt, O., Pierneef, R., Mncube, K., Lima-Mendez, G. & Reva, O. N. Mainstreams of horizontal gene exchange in enterobacteria: Consideration of the outbreak of enterohemorrhagic E. coli O104:H4 in Germany in 2011. PLoS One 6, e25702 (2011).
14. Langille, M. G. & Brinkman, F. S. IslandViewer: An integrated interface for computational identification and visualization of genomic islands. Bioinformatics 25, 664-665 (2009).
15. Menigaud, S. et al. GOHTAM: A website for genomic origin of horizontal transfers, alignment and metagenomics. Bioinformatics 28, 1270-1271 (2012).
16. Pierneef, R., Cronje, L., Bezuidt, O. & Reva, O. N. Pre GI: A global map of ontological links between horizontally transferred genomic islands in bacterial and archaeal genomes. Database (Oxford):bav058 (2015).
17. Lin, Z., Nei, M. & Ma, H. The origins and early evolution of DNA mismatch repair genes multiple horizontal gene transfers and coevolution. Nucl Acids Res 35, 7591-7603 (2007).
18. Filee, J., Siguier, P. & Chandler, M. Insertion Sequence Diversity in Archaea. Microbiol Mol Biol Rev 71, 121-157 (2007).
19. Haldenby, S., White, M. F. & Allers, T. RecA family proteins in archaea: RadA and its cousins. Biochem Soc Trans 37(Pt 1), 102 (2009).
20. Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I. & Koonin, E. V. A putative RNA-interference-based immune system in prokaryotes: Computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 16, 7 (2006).
21. Tyson, G. W. & Banfield, J. F. Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 1, 200-207 (2008).
22. Gophna, U. et al. No evidence of inhibition of horizontal gene transfer by CRISPR-Cas on evolutionary timescales. ISME J 9, 2021-2027 (2015).
23. Makarova, K. S. et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9, 467-477 (2011).
24. Deng, L., Garret, R. A., Shah, S. A., Peng, X. & She, Q. A novel interference mechanism by a type IIIB CRISPR-Cmr module in Sulfolobus. Mol Microbiol 87, 1088-1099 (2013).
25. Wiedenheft, B., Sternberg, S. H. & Doudna, J. A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482, 331-338 (2012).
26. Lynch, M. Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci USA 107, 961-968 (2010).
27. Sung, W., Ackerman, M. S., Miller, S. F., Doak, T. G. & Lynch, M. Drift-barrier hypothesis and mutation-rate evolution. Proc Natl Acad Sci USA 109, 18488-18492 (2012).
28. Tompkins, J. D. et al. Error-prone polymerase, DNA polymerase IV, is responsible for transient hypermutation during adaptive mutation in Escherichia coli. J Bacteriol 185, 3469-3472 (2003).
29. Castelle, C. J. et al. The aerobic respiratory chain of the acidophilic archaeon Ferroplasma acidiphilum: A membrane-bound complex oxidizing ferrous iron. Biochim Biophys Acta 1847, 717-728 (2015).
30. Futterer, O. et al. Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci USA 101, 9091-9096 (2004).
31. Golyshina, O. V. et al. Biology of archaea from a novel family Cuniculiplasmataceae (Thermoplasmata) ubiquitous in hyperacidic environments. SciRep 6, 39034 (2016).
32. Soppa, J., Vatter, P., zur Miihlen, A., Link, T. & Ruepp, A. Regulation of Gene Expression in Halobacterium salinarum: The arcrACB Gene Cluster and the TATA box-binding protein. In: Oren A (ed.) Microbiology and Biogeochemistry of Hypersaline Environments 5, 249-263 (1998).
33. Zuniga, M., Perez, G. & Gonzalez-Candelas, F. Evolution of arginine deiminase (ADI) pathway genes. Mol Phylogenet Evol 25, 429-444 (2002).
34. Xiong, L. et al. Arginine deiminase pathway is far more important than urease for acid resistance and intracellular survival in Laribacter hongkongensis: A possible result of arc gene cassette duplication. BMC Microbiol 14, 1 (2014).
35. Sousa, F. L., Alves, R. J., Pereira-Leal, J. B., Teixeira, M. & Pereira, M. M. A bioinformatics classifier and database for heme-copper oxygen reductases. PLoS One 6, e19117 (2011).
36. Sousa, F. L., Nelson-Sathi, S. & Martin, W. F. One step beyond a ribosome: The ancient anaerobic core. Biochim Biophys Acta 1857, 1027-1038 (2016).
37. Lane, N. & Martin, W. F. The origin of membrane bioenergetics. Cell 151, 1406-1416 (2012).
38. Adams, M. W. & Kletzin, A. Oxidoreductase-type enzymes and redox proteins involved in fermentative metabolisms of hyperthermophilic archaea. Adv Protein Chem 48, 101-180 (1996).
39. Ng, W. V. et al. Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97, 12176-81 (2000).
40. Kerscher, L. & Oesterhelt, D. The catalytic mechanism of 2aoxoacid: ferredoxin oxidoreductases from Halobacterium halobium. European J Biochem 116, 595-600 (1981).
41. Kawasumi, T., Igarashi, Y., Kodama, T. & Minoda, Y. Hydrogenobacter thermophilus gen. nov., sp. nov., an extremely thermophilic, aerobic, hydrogen-oxidizing bacterium. Int J Syst Bacteriol 34, 5-10 (1984).
42. Ikeda, T. et al. Enzymatic and electron paramagnetic resonance studies of anabolic pyruvate synthesis by pyruvate: ferredoxin oxidoreductase from Hydrogenobacter thermophilus. FEBS J 277, 501-510 (2010).
43. Yamamoto, M., Ikeda, T., Arai, H., Ishii, M. & Igarashi, Y. Carboxylation reaction catalyzed by 2-oxoglutarate:ferredoxin oxidoreductases from Hydrogenobacter thermophilus. Extremophiles 14, 79-85 (2010).
44. Yoon, K. S., Ishii, M., Igarashi, Y. & Kodama, T. Purification and characterization of 2-oxoglutarate: ferredoxin oxidoreductase from a thermophilic, obligately chemolithoautotrophic bacterium, Hydrogenobacter thermophilus TK-6. J Bacteriol 178, 3365-3368 (1996).
45. Blaut, M. Metabolism of methanogens. Antonie Van Leeuwenhoek 66, 187-208 (1994).
46. Dopson, M., Baker-Austin, C. & Bond, P. Towards determining details of anaerobic growth coupled to ferric iron reduction by the acidophilic archaeon 'Ferroplasma acidarmanus' Fer1. Extremophiles 11, 159-168 (2007).
47. Baker-Austin, C., Potrykus, J., Wexler, M., Bond, P. L. & Dopson, M. Biofilm development in the extremely acidophilic archaeon 'Ferroplasma acidarmanus' Fer1. Extremophiles 6, 485-491 (2010).
48. Danson, M. J., Lamble, H. J. & Hough, D. W. Central metabolism. In: Cavicchioli R. (ed). Archaea: Molecular and Cellular Biology. Washington DC: ASM Press, pp. 260-287 (2007).
49. Say, R. F. & Fuchs, G. Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077-1081 (2010).
50. Mwirichia, R. et al. Metabolic traits of an uncultured archaeal lineage-MSBL1-from brine pools of the Red Sea. Sci Rep 6, 19181 (2016).
51. Pivovarova, T. A. et al. Phenotypic features of Ferroplasma acidiphilum strains Yt and Y-2. Mikrobiologiia 71, 809-818 (2002).
52. Pao, S. S., Paulsen, I. T. & Saier, M. H. Major facilitator superfamily. Microbiol Mol Biol Rev 62, 1-34 (1998).
53. Dias, P. J. & Sa-Correia, I. The drug:H+ antiporters of family 2 (DHA2), siderophore transporters (ARN) and glutathione:H+antiporters (GEX) have a common evolutionary origin in hemiascomycete yeasts. BMC Genomics 14, 901 (2013).
54. Gough, J., Karplus, K., Hughey, R. & Chothia, C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313, 903-919 (2001).
55. Tamura, N., Lottspeich, F., Baumeister, W. & Tamura, T. The role of tricorn protease and its aminopeptidase-interacting factors in cellular protein degradation. Cell 95, 637-648 (1998).
56. Schonheit, P., Buckel, W. & Martin, W. F. On the origin of heterotrophy. Trends in Microbiol 24, 12-25 (2016).
57. Ewing, B., Hiller, L., Wendt, M. C. & Green, P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8, 175-185 (1998).
58. Ewing, B. & Green, P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8, 186-194 (1998).
59. Gordon, D. Viewing and editing assembled sequences using Consed. Curr Protoc Bioinformatics 2, 11.2.1-11.2.43 (2003).
60. Han, C. S. & Chain, P. Finishing repetitive regions automatically with Dupfinisher. In: Arabnia HR Valafar H. (eds). Proceedings of the 2006 International Conference on Bioinformatics and Computational Biology. Las Vegas, NV, USA: CSREA Press, pp. 142-147 (2006).
61. Malykh, A., Malykh, O., Polushin, N., Kozyavkin, S. & Slesarev, A. Finishing 'Working Draft' BAC projects by directed sequencing with ThermoFidelase and Fimers. Method Mol Biol 255, 295-308 (2004).
62. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J Mol Biol 215, 403-410 (1990).
63. Schattner, P., Brooks, A. N. & Lowe, T. M. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33, W686-689 (2005).
64. Grissa, I., Vergnaud, G. & Pourcel, C. CRISPRFinder: A web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35, W 52-57 (2007).
65. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(aaaCt) method. Methods 25, 402-408 (2001).
66. Bron, P. A. et al. Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J Bacteriol 186, 7829-7835 (2004).
67. Marco, M. L., Bongers, R. S., de Vos, W. M. & Kleerebezem, M. Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. Appl Environ Microbiol 73, 124-132 (2007).
68. Ganesan, H., Rakitianskaia, A. S., Davenport, C. F., Tummler, B. & Reva, O. N. The SeqWord Genome Browser: An online tool for the identification and visualization of atypical regions of bacterial genomes through oligonucleotide usage. BMC Bioinformatics 9, 333 (2008).